Phase separation organizes the site of autophagosome formation

Many biomolecules undergo liquid–liquid phase separation to form liquid-like condensates that mediate diverse cellular functions 1 , 2 . Autophagy is able to degrade such condensates using autophagosomes—double-membrane structures that are synthesized de novo at the pre-autophagosomal structure (PAS...

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Veröffentlicht in:	Nature (London) Jg. 578; H. 7794; S. 301 - 305
Hauptverfasser:	Fujioka, Yuko, Alam, Jahangir Md, Noshiro, Daisuke, Mouri, Kazunari, Ando, Toshio, Okada, Yasushi, May, Alexander I., Knorr, Roland L., Suzuki, Kuninori, Ohsumi, Yoshinori, Noda, Nobuo N.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	London Nature Publishing Group UK 13.02.2020 Nature Publishing Group
Schlagworte:	13/1 14/19 14/33 14/35 631/57/2267 631/80/39 631/80/458 82/83 Adaptor Proteins, Signal Transducing - chemistry Adaptor Proteins, Signal Transducing - genetics Adaptor Proteins, Signal Transducing - metabolism Autophagosomes - chemistry Autophagosomes - metabolism Autophagy Autophagy (Cytology) Autophagy-Related Proteins - chemistry Autophagy-Related Proteins - genetics Autophagy-Related Proteins - metabolism Biomolecules Condensates Droplets Experiments Fragility Humanities and Social Sciences Kinases Liquid phases Localization Mechanistic Target of Rapamycin Complex 1 - chemistry Mechanistic Target of Rapamycin Complex 1 - metabolism Membrane structures Membranes Microscopy multidisciplinary Multiprotein Complexes - chemistry Multiprotein Complexes - genetics Multiprotein Complexes - metabolism Mutation Observations Phagocytosis Phagosomes Phase separation Phase transformations (Statistical physics) Phosphorylation Physiological aspects Point Mutation Protein Binding Protein interaction Protein Kinases - chemistry Protein Kinases - genetics Protein Kinases - metabolism Proteins Saccharomyces cerevisiae - chemistry Saccharomyces cerevisiae - cytology Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae - metabolism Saccharomyces cerevisiae Proteins - chemistry Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - metabolism Science Science (multidisciplinary) Vacuoles - metabolism Yeast fungi Japan
ISSN:	0028-0836, 1476-4687, 1476-4687
Online-Zugang:	Volltext
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Abstract	Many biomolecules undergo liquid–liquid phase separation to form liquid-like condensates that mediate diverse cellular functions 1 , 2 . Autophagy is able to degrade such condensates using autophagosomes—double-membrane structures that are synthesized de novo at the pre-autophagosomal structure (PAS) in yeast 3 – 5 . Whereas Atg proteins that associate with the PAS have been characterized, the physicochemical and functional properties of the PAS remain unclear owing to its small size and fragility. Here we show that the PAS is in fact a liquid-like condensate of Atg proteins. The autophagy-initiating Atg1 complex undergoes phase separation to form liquid droplets in vitro, and point mutations or phosphorylation that inhibit phase separation impair PAS formation in vivo. In vitro experiments show that Atg1-complex droplets can be tethered to membranes via specific protein–protein interactions, explaining the vacuolar membrane localization of the PAS in vivo. We propose that phase separation has a critical, active role in autophagy, whereby it organizes the autophagy machinery at the PAS. The pre-autophagosomal structure in yeast is a liquid-like condensate of Atg proteins whose phase separation may have a critical, active role in autophagy.
AbstractList	Many biomolecules undergo liquid-liquid phase separation to form liquid-like condensates that mediate diverse cellular functions1,2. Autophagy is able to degrade such condensates using autophagosomes-double-membrane structures that are synthesized de novo at the pre-autophagosomal structure (PAS) in yeast3-5. Whereas Atg proteins that associate with the PAS have been characterized, the physicochemical and functional properties of the PAS remain unclear owing to its small size and fragility. Here we show that the PAS is in fact a liquid-like condensate of Atg proteins. The autophagy-initiating Atgl complex undergoes phase separation to form liquid droplets in vitro, and point mutations or phosphorylation that inhibit phase separation impair PAS formation in vivo. In vitro experiments show that Atgl-complex droplets can be tethered to membranes via specific protein-protein interactions, explaining the vacuolar membrane localization of the PAS in vivo. We propose that phase separation has a critical, active role in autophagy, whereby it organizes the autophagy machinery at the PAS. Many biomolecules undergo liquid-liquid phase separation to form liquid-like condensates that mediate diverse cellular functions.sup.1,2. Autophagy is able to degrade such condensates using autophagosomes--double-membrane structures that are synthesized de novo at the pre-autophagosomal structure (PAS) in yeast.sup.3-5. Whereas Atg proteins that associate with the PAS have been characterized, the physicochemical and functional properties of the PAS remain unclear owing to its small size and fragility. Here we show that the PAS is in fact a liquid-like condensate of Atg proteins. The autophagy-initiating Atg1 complex undergoes phase separation to form liquid droplets in vitro, and point mutations or phosphorylation that inhibit phase separation impair PAS formation in vivo. In vitro experiments show that Atg1-complex droplets can be tethered to membranes via specific protein-protein interactions, explaining the vacuolar membrane localization of the PAS in vivo. We propose that phase separation has a critical, active role in autophagy, whereby it organizes the autophagy machinery at the PAS. Many biomolecules undergo liquid–liquid phase separation to form liquid-like condensates that mediate diverse cellular functions 1 , 2 . Autophagy is able to degrade such condensates using autophagosomes—double-membrane structures that are synthesized de novo at the pre-autophagosomal structure (PAS) in yeast 3 – 5 . Whereas Atg proteins that associate with the PAS have been characterized, the physicochemical and functional properties of the PAS remain unclear owing to its small size and fragility. Here we show that the PAS is in fact a liquid-like condensate of Atg proteins. The autophagy-initiating Atg1 complex undergoes phase separation to form liquid droplets in vitro, and point mutations or phosphorylation that inhibit phase separation impair PAS formation in vivo. In vitro experiments show that Atg1-complex droplets can be tethered to membranes via specific protein–protein interactions, explaining the vacuolar membrane localization of the PAS in vivo. We propose that phase separation has a critical, active role in autophagy, whereby it organizes the autophagy machinery at the PAS. The pre-autophagosomal structure in yeast is a liquid-like condensate of Atg proteins whose phase separation may have a critical, active role in autophagy. Many biomolecules undergo liquid-liquid phase separation to form liquid-like condensates that mediate diverse cellular functions.sup.1,2. Autophagy is able to degrade such condensates using autophagosomes--double-membrane structures that are synthesized de novo at the pre-autophagosomal structure (PAS) in yeast.sup.3-5. Whereas Atg proteins that associate with the PAS have been characterized, the physicochemical and functional properties of the PAS remain unclear owing to its small size and fragility. Here we show that the PAS is in fact a liquid-like condensate of Atg proteins. The autophagy-initiating Atg1 complex undergoes phase separation to form liquid droplets in vitro, and point mutations or phosphorylation that inhibit phase separation impair PAS formation in vivo. In vitro experiments show that Atg1-complex droplets can be tethered to membranes via specific protein-protein interactions, explaining the vacuolar membrane localization of the PAS in vivo. We propose that phase separation has a critical, active role in autophagy, whereby it organizes the autophagy machinery at the PAS. The pre-autophagosomal structure in yeast is a liquid-like condensate of Atg proteins whose phase separation may have a critical, active role in autophagy. Many biomolecules undergo liquid-liquid phase separation to form liquid-like condensates that mediate diverse cellular functions . Autophagy is able to degrade such condensates using autophagosomes-double-membrane structures that are synthesized de novo at the pre-autophagosomal structure (PAS) in yeast . Whereas Atg proteins that associate with the PAS have been characterized, the physicochemical and functional properties of the PAS remain unclear owing to its small size and fragility. Here we show that the PAS is in fact a liquid-like condensate of Atg proteins. The autophagy-initiating Atg1 complex undergoes phase separation to form liquid droplets in vitro, and point mutations or phosphorylation that inhibit phase separation impair PAS formation in vivo. In vitro experiments show that Atg1-complex droplets can be tethered to membranes via specific protein-protein interactions, explaining the vacuolar membrane localization of the PAS in vivo. We propose that phase separation has a critical, active role in autophagy, whereby it organizes the autophagy machinery at the PAS. Many biomolecules undergo liquid-liquid phase separation to form liquid-like condensates that mediate diverse cellular functions1,2. Autophagy is able to degrade such condensates using autophagosomes-double-membrane structures that are synthesized de novo at the pre-autophagosomal structure (PAS) in yeast3-5. Whereas Atg proteins that associate with the PAS have been characterized, the physicochemical and functional properties of the PAS remain unclear owing to its small size and fragility. Here we show that the PAS is in fact a liquid-like condensate of Atg proteins. The autophagy-initiating Atg1 complex undergoes phase separation to form liquid droplets in vitro, and point mutations or phosphorylation that inhibit phase separation impair PAS formation in vivo. In vitro experiments show that Atg1-complex droplets can be tethered to membranes via specific protein-protein interactions, explaining the vacuolar membrane localization of the PAS in vivo. We propose that phase separation has a critical, active role in autophagy, whereby it organizes the autophagy machinery at the PAS.Many biomolecules undergo liquid-liquid phase separation to form liquid-like condensates that mediate diverse cellular functions1,2. Autophagy is able to degrade such condensates using autophagosomes-double-membrane structures that are synthesized de novo at the pre-autophagosomal structure (PAS) in yeast3-5. Whereas Atg proteins that associate with the PAS have been characterized, the physicochemical and functional properties of the PAS remain unclear owing to its small size and fragility. Here we show that the PAS is in fact a liquid-like condensate of Atg proteins. The autophagy-initiating Atg1 complex undergoes phase separation to form liquid droplets in vitro, and point mutations or phosphorylation that inhibit phase separation impair PAS formation in vivo. In vitro experiments show that Atg1-complex droplets can be tethered to membranes via specific protein-protein interactions, explaining the vacuolar membrane localization of the PAS in vivo. We propose that phase separation has a critical, active role in autophagy, whereby it organizes the autophagy machinery at the PAS.
Audience	Academic
Author	Mouri, Kazunari Ohsumi, Yoshinori Ando, Toshio Fujioka, Yuko Noshiro, Daisuke May, Alexander I. Okada, Yasushi Alam, Jahangir Md Knorr, Roland L. Noda, Nobuo N. Suzuki, Kuninori
Author_xml	– sequence: 1 givenname: Yuko surname: Fujioka fullname: Fujioka, Yuko organization: Institute of Microbial Chemistry (BIKAKEN) – sequence: 2 givenname: Jahangir Md surname: Alam fullname: Alam, Jahangir Md organization: Institute of Microbial Chemistry (BIKAKEN) – sequence: 3 givenname: Daisuke surname: Noshiro fullname: Noshiro, Daisuke organization: Institute of Microbial Chemistry (BIKAKEN), Nano Life Science Institute (WPI-NanoLSI), Kanazawa University – sequence: 4 givenname: Kazunari surname: Mouri fullname: Mouri, Kazunari organization: Center for Biosystems Dynamics Research (BDR), RIKEN – sequence: 5 givenname: Toshio surname: Ando fullname: Ando, Toshio organization: Nano Life Science Institute (WPI-NanoLSI), Kanazawa University – sequence: 6 givenname: Yasushi surname: Okada fullname: Okada, Yasushi organization: Center for Biosystems Dynamics Research (BDR), RIKEN, Department of Physics, Universal Biology Institute (UBI) and International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo – sequence: 7 givenname: Alexander I. surname: May fullname: May, Alexander I. organization: Cell Biology Center, Institute of Innovative Research, Tokyo Institute of Technology, Tokyo Tech World Research Hub Initiative (WRHI), Institute of Innovative Research, Tokyo Institute of Technology – sequence: 8 givenname: Roland L. surname: Knorr fullname: Knorr, Roland L. organization: Department of Theory and Bio-Systems, Max Planck Institute of Colloids and Interfaces, Graduate School and Faculty of Medicine, The University of Tokyo, Max Planck Institute of Molecular Plant Physiology – sequence: 9 givenname: Kuninori surname: Suzuki fullname: Suzuki, Kuninori organization: Life Science Data Research Center, Graduate School of Frontier Sciences, The University of Tokyo, Collaborative Research Institute for Innovative Microbiology, The University of Tokyo – sequence: 10 givenname: Yoshinori surname: Ohsumi fullname: Ohsumi, Yoshinori organization: Cell Biology Center, Institute of Innovative Research, Tokyo Institute of Technology – sequence: 11 givenname: Nobuo N. surname: Noda fullname: Noda, Nobuo N. email: nn@bikaken.or.jp organization: Institute of Microbial Chemistry (BIKAKEN)
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/32025038$$D View this record in MEDLINE/PubMed
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Snippet	Many biomolecules undergo liquid–liquid phase separation to form liquid-like condensates that mediate diverse cellular functions 1 , 2 . Autophagy is able to... Many biomolecules undergo liquid-liquid phase separation to form liquid-like condensates that mediate diverse cellular functions . Autophagy is able to degrade... Many biomolecules undergo liquid-liquid phase separation to form liquid-like condensates that mediate diverse cellular functions.sup.1,2. Autophagy is able to... Many biomolecules undergo liquid-liquid phase separation to form liquid-like condensates that mediate diverse cellular functions1,2. Autophagy is able to...
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Title	Phase separation organizes the site of autophagosome formation
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